Bauer Eugen, Salem Hassan, Marz Manja, Vogel Heiko, Kaltenpoth Martin
Insect Symbiosis Research Group, Max Planck Institute for Chemical Ecology, Jena, 07745, Germany.
Faculty of Mathematics and Computer Science, Friedrich Schiller University, Jena, 07743, Germany.
PLoS One. 2014 Dec 9;9(12):e114865. doi: 10.1371/journal.pone.0114865. eCollection 2014.
The acquisition and vertical transmission of bacterial symbionts plays an important role in insect evolution and ecology. However, the molecular mechanisms underlying the stable maintenance and control of mutualistic bacteria remain poorly understood. The cotton stainer Dysdercus fasciatus harbours the actinobacterial symbionts Coriobacterium glomerans and Gordonibacter sp. in its midgut. The symbionts supplement limiting B vitamins and thereby significantly contribute to the host's fitness. In this study, we experimentally disrupted the symbionts' vertical transmission route and performed comparative transcriptomic analyses of genes expressed in the gut of aposymbiotic (symbiont-free) and control individuals to study the host immune response in presence and absence of the mutualists. Annotation of assembled cDNA reads identified a considerable number of genes involved in the innate immune system, including different protein isoforms of several immune effector proteins (specifically i-type lysozyme, defensin, hemiptericin, and pyrrhocoricin), suggesting the possibility for a highly differentiated response towards the complex resident microbial community. Gene expression analyses revealed a constitutive expression of transcripts involved in signal transduction of the main insect immune pathways, but differential expression of certain antimicrobial peptide genes. Specifically, qPCRs confirmed the significant down-regulation of c-type lysozyme and up-regulation of hemiptericin in aposymbiotic individuals. The high expression of c-type lysozyme in symbiont-containing bugs may serve to lyse symbiont cells and thereby harvest B-vitamins that are necessary for subsistence on the deficient diet of Malvales seeds. Our findings suggest a sophisticated host response to perturbation of the symbiotic gut microbiota, indicating that the innate immune system not only plays an important role in combating pathogens, but also serves as a communication interface between host and symbionts.
细菌共生体的获取和垂直传播在昆虫进化和生态中起着重要作用。然而，互利共生细菌稳定维持和调控的分子机制仍知之甚少。棉红蝽（Dysdercus fasciatus）的中肠内含有放线菌共生体球状棒状杆菌（Coriobacterium glomerans）和戈登氏菌属（Gordonibacter sp.）。这些共生体补充宿主有限的B族维生素，从而显著促进宿主的健康。在本研究中，我们通过实验破坏了共生体的垂直传播途径，并对无菌共生体（无共生体）和对照个体肠道中表达的基因进行了比较转录组分析，以研究宿主在有无共生体情况下的免疫反应。对组装的cDNA读数进行注释，确定了大量参与先天免疫系统的基因，包括几种免疫效应蛋白的不同蛋白异构体（特别是i型溶菌酶、防御素、半翅菌素和红蝽菌素），这表明对复杂的常驻微生物群落可能存在高度分化的反应。基因表达分析揭示了参与主要昆虫免疫途径信号转导的转录本的组成型表达，但某些抗菌肽基因存在差异表达。具体而言，qPCR证实无菌共生体个体中c型溶菌酶显著下调，半翅菌素上调。含共生体的虫子中c型溶菌酶的高表达可能用于裂解共生体细胞，从而获取锦葵科种子缺乏的饮食中生存所需的B族维生素。我们的研究结果表明宿主对共生肠道微生物群的扰动有复杂的反应，这表明先天免疫系统不仅在对抗病原体中起重要作用，而且还作为宿主与共生体之间的通讯界面。
